Gestational hypoxia induces preeclampsia-like symptoms via heightened endothelin-1 signaling in pregnant rats

Hypertension. 2013 Sep;62(3):599-607. doi: 10.1161/HYPERTENSIONAHA.113.01449. Epub 2013 Jul 1.

Abstract

Preeclampsia is a life-threatening pregnancy disorder. However, its pathogenesis remains unclear. We tested the hypothesis that gestational hypoxia induces preeclampsia-like symptoms via heightened endothelin-1 (ET-1) signaling. Time-dated pregnant and nonpregnant rats were divided into normoxic and hypoxic (10.5% O2 from the gestational day 6-21) groups. Chronic hypoxia had no significant effect on blood pressure or proteinuria in nonpregnant rats but significantly increased blood pressure on day 12 (systolic blood pressure, 111.7 ± 6.1 versus 138.5 ± 3.5 mm Hg; P=0.004) and day 20 (systolic blood pressure, 103.4 ± 4.6 versus 125.1 ± 6.1 mm Hg; P=0.02) in pregnant rats and urine protein (μg/μL)/creatinine (nmol/μL) ratio on day 20 (0.10 ± 0.01 versus 0.20 ± 0.04; P=0.04), as compared with the normoxic control group. This was accompanied with asymmetrical fetal growth restriction. Hypoxia resulted in impaired trophoblast invasion and uteroplacental vascular remodeling. In addition, plasma ET-1 levels, as well as the abundance of prepro-ET-1 mRNA, ET-1 type A receptor and angiotensin II type 1 receptor protein in the kidney and placenta were significantly increased in the chronic hypoxic group, as compared with the control animals. Treatment with the ET-1 type A receptor antagonist, BQ123, during the course of hypoxia exposure significantly attenuated the hypoxia-induced hypertension and other preeclampsia-like features. The results demonstrate that chronic hypoxia during gestation induces preeclamptic symptoms in pregnant rats via heightened ET-1 and ET-1 type A receptor-mediated signaling, providing a molecular mechanism linking gestational hypoxia and increased risk of preeclampsia.

Keywords: angiotensin II type I receptor; anoxia; endothelin-1; hypertension; preeclampsia; receptor, endothelin A.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blood Pressure / drug effects
  • Blood Pressure / physiology*
  • Disease Models, Animal
  • Endothelin A Receptor Antagonists
  • Endothelin-1 / blood*
  • Female
  • Hypoxia / complications
  • Hypoxia / metabolism*
  • Hypoxia / physiopathology
  • Hypoxia-Inducible Factor 1, alpha Subunit / genetics
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism
  • Kidney / drug effects
  • Kidney / metabolism
  • Kidney / physiopathology
  • Peptides, Cyclic / pharmacology
  • Placenta / metabolism
  • Pre-Eclampsia / etiology
  • Pre-Eclampsia / metabolism*
  • Pre-Eclampsia / physiopathology
  • Pregnancy
  • Proteinuria / etiology
  • Proteinuria / metabolism
  • Proteinuria / physiopathology
  • Rats
  • Rats, Sprague-Dawley
  • Receptor, Angiotensin, Type 1 / genetics
  • Receptor, Angiotensin, Type 1 / metabolism
  • Signal Transduction / drug effects
  • Signal Transduction / physiology*

Substances

  • Endothelin A Receptor Antagonists
  • Endothelin-1
  • Hif1a protein, rat
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Peptides, Cyclic
  • Receptor, Angiotensin, Type 1
  • cyclo(Trp-Asp-Pro-Val-Leu)